Seed-dispersal Networks Research Articles

Seed Dispersal Networks in Neotropical Forest Areas of the Amazon, Cerrado, and Associated Ecotone: Abundance as the Driver of Bat Roles

Seed Dispersal Networks in Neotropical Forest Areas of the Amazon, Cerrado, and Associated Ecotone: Abundance as the Driver of Bat Roles

Structure and vulnerability of the ichthyochory network in wetland forests of Central Amazonia

AbstractThe interaction between fish and plants is vital for the dynamics of ecosystems since it influences plant distribution and regeneration patterns. In the floodable areas of the Amazon, these interactions are mainly structured by the flood pulse, which enables seed dispersal via water (hydrochory) and fish (ichthyochory), and which contributes to the formation of complex mutualistic networks. Our study evaluated the structure (modularity, nestedness, specialisation, and robustness) of the network of dispersal of seeds by frugivorous fish in a floodplain forest in Central Amazonia. We expect the binary network to have a nested pattern, while the weighted network is expected to have a non‐nested structure; that generalist frugivorous species should constitute the core of the network, while specialist frugivorous species will be peripheral; that the size of fish and seeds is related to specialisation, and that the robustness of the network weakens as generalist frugivorous fish are removed. We found 5012 intact seeds from 49 plant species in the digestive tracts of 11 species of frugivorous fish. A nested and modular pattern was found for the binary and weighted networks, albeit with a low degree of nestedness. Our network proved relatively robust when the frugivores were removed, whereby all the fish and plant species became peripheral. No relationship was found between the size of the fish and the seeds and the degree of specialisation. Considering the anthropogenic impacts that can cause modifications in seed dispersal networks, knowing the structure of mutualistic networks is fundamental in order to be able infer the vulnerability of the interactions as a result of changes in the ecosystem.

Frugivore-mediated seed dispersal in fragmented landscapes: Compositional and functional turnover from forest to matrix.

Seed dispersal by frugivores is a fundamental function for plant community dynamics in fragmented landscapes, where forest remnants are typically embedded in a matrix of anthropogenic habitats. Frugivores can mediate both connectivity among forest remnants and plant colonization of the matrix. However, it remains poorly understood how frugivore communities change from forest to matrix due to the loss or replacement of species with traits that are less advantageous in open habitats and whether such changes ultimately influence the composition and traits of dispersed plants via species interactions. Here, we close this gap by using a unique dataset of seed-dispersal networks that were sampled in forest patches and adjacent matrix habitats of seven fragmented landscapes across Europe. We found a similar diversity of frugivores, plants, and interactions contributing to seed dispersal in forest and matrix, but a high turnover (replacement) in all these components. The turnover of dispersed seeds was smaller than that of frugivore communities because different frugivore species provided complementary seed dispersal in forest and matrix. Importantly, the turnover involved functional changes toward larger and more mobile frugivores in the matrix, which dispersed taller, larger-seeded plants with later fruiting periods. Our study provides a trait-based understanding of frugivore-mediated seed dispersal through fragmented landscapes, uncovering nonrandom shifts that can have cascading consequences for the composition of regenerating plant communities. Our findings also highlight the importance of forest remnants and frugivore faunas for ecosystem resilience, demonstrating a high potential for passive forest restoration of unmanaged lands in the matrix.

The reliability of regional ecological knowledge to build local interaction networks: a test using seed-dispersal networks across land-bridge islands.

Building ecological networks is the fundamental basis of depicting how species in communities interact, but sampling complex interaction networks is extremely labour intensive. Recently, indirect ecological information has been applied to build interaction networks. Here we propose to extend the source of indirect ecological information, and applied regional ecological knowledge to build local interaction networks. Using a high-resolution dataset consisting of 22 locally observed networks with 17 572 seed-dispersal events, we test the reliability of indirectly derived local networks based on regional ecological knowledge (REK) across islands. We found that species richness strongly influenced 'local interaction rewiring' (i.e. the proportion of locally observed interactions among regionally interacting species), and all network properties were biased using REK-based networks. Notably, species richness and local interaction rewiring strongly affected estimations of REK-based network structures. However, locally observed and REK-based networks detected the same trends of how network structure correlates to island area and isolation. These results suggest that we should use REK-based networks cautiously for reflecting actual interaction patterns of local networks, but highlight that REK-based networks have great potential for comparative studies across environmental gradients. The use of indirect regional ecological information may thus advance our understanding of biogeographical patterns of species interactions.

Species-level drivers of avian centrality within seed-dispersal networks across different levels of organisation.

Bird-plant seed-dispersal networks are structural components of ecosystems. The role of bird species in seed-dispersal networks (from less [peripheral] to more connected [central]), determines the interaction patterns and their ecosystem services. These roles may be driven by morphological and functional traits as well as evolutionary, geographical and environmental properties acting at different spatial extents. It is still unknown if such drivers are equally important in determining species centrality at different network levels, from individual local networks to the global meta-network representing interactions across all local networks. Using 308 networks covering five continents and 11 biogeographical regions, we show that at the global meta-network level species' range size was the most important driver of species centrality, with more central species having larger range sizes, which would facilitate the interaction with a higher number of plants and thus the maintenance of seed-dispersal interactions. At the local network level, body mass was the only driver with a significant effect, implying that local factors related to resource availability are more important at this level of network organisation than those related to broad spatial factors such as range sizes. This could also be related to the mismatch between species-level traits, which do not consider intraspecific variation, and the local networks that can depend on such variation. Taken together, our results show that the drivers determining species centrality are relative to the levels of network organisation, suggesting that prediction of species functional roles in seed-dispersal interactions requires combined local and global approaches.

Effects of plant species richness on the structure of plant-bird interaction networks along a 3000-m elevational gradient in subtropical forests

Ecological community diversity and structure has implications for bird seed-dispersal networks that change with environmental conditions and plant species richness along elevational gradients. In this study, we examined how plant-bird interactions change with plant species richness at both the network and species level, along a 3000-m elevational gradient in a subtropical forest ecosystem. At the network level, Shannon diversity interactions (H2) decreased consistently with elevation, with a concomitant decrease in network specialization (H2′), likely due to lower plant and bird species richness at higher elevations. At the species level, the number of effective partners for both plants and birds decreased with increasing elevation, while the degree of specialization of both plants and birds on their partners increased with elevation. Specifically, we found a unimodal pattern where the effective partners of both birds and plants initially increased and then decreased with plant species richness. Furthermore, we found an inverted unimodal relationship between the degree of specialization and plant species richness, where the degree of specialization between birds and plants initially decreased and then increased with plant species richness. This study provides the first empirical evidence that changes in plant species richness with elevation can affect plant-bird interaction networks in subtropical forests.

Abundance and trait-matching both shape interaction frequencies between plants and birds in seed-dispersal networks

Abundance and trait-driven processes have both been identified as potential mechanisms in determining the occurrence of species interactions. However, little is known about how these two mechanisms interact to determine the relative frequencies of interactions between species, and thereby species-specific contributions to ecological functions. Here, we evaluate the effect of both species’ abundance and trait-matching on the occurrence of plant-bird seed dispersal interactions in the Cantabrian Range (northern Spain). For two years at fourteen plots, we independently sampled the abundance and diversity of fleshy-fruited plants and frugivores, as well as the consumption of fruits by birds. We quantified trait-matching by applying a food-web approach based on the log-ratios of species traits relevant to seed dispersal and traits related to fruit-handling and foraging-stratum. We fitted multi-level models incorporating phylogenetic relatedness to identify phylogenetically independent effects of species abundance and trait-matching on interaction frequencies. Fitted models showed that species abundances of both plants and birds always had strong positive effects on interaction frequencies. Trait-matching effects associated with fruit-handling were weak, but consistent across years, whereas those derived from foraging stratum varied across years, according to strong interannual changes in species abundance. Our findings reveal that both species abundance and functional traits are required for a mechanistic understanding of species interactions, as well as for predicting species roles in ecosystems under global change.

Long-term dynamics of the network structures in seed dispersal associated with fluctuations in bird migration and fruit abundance patterns.

In temperate zones, seed-dispersal networks by migratory birds are formed on long time scale. In mid-October from 2005 to 2016, to explore the dynamics of the network structures, we examined interannual variability of fruit abundance, bird migration, and seed-dispersal networks in central Japan. For 12years, the fruit abundance exhibited a remarkable fluctuation across years, with the number of fruiting plants and matured fruits fluctuating repeatedly every other year, leading to the periodic fluctuations. The abundance of migratory birds was also fluctuated. According to the abundance of fruits and migratory birds, the 12years was classified into three types: frugivores and fruits were abundant, frugivores were abundant but fruits were scarce, and frugivores were scarce. The seed-dispersal networks were investigated by collecting faeces and vomits of migrants. Of the 6652 samples collected from 15 bird species, 1671 (25.1%) included seeds from 60 plant species. Main dispersers were composed of Turdus pallidus, T. obscurus, and Zosterops japonicus. The network structures were almost nested for 12years. Specifically, the nested structure was developed in years when fruit abundance was low. GLM analyses showed the abundance of migrants, particularly T. pallidus and T. obscurus, had strong positive effects on nested structure. It may be caused by the fact the two Turdus species were more frequently functioning as generalist dispersers when fruit abundance was lower. Our study suggested fruit abundance and foraging behaviour of frugivores determine the network structures of seed dispersal on long time scale.

Disruption of a Keystone Interaction Erodes Pollination and Seed Dispersal Networks

Disruption of a Keystone Interaction Erodes Pollination and Seed Dispersal Networks

Structure-based identification of sensor species for anticipating critical transitions

Ecological systems can undergo sudden, catastrophic changes known as critical transitions. Anticipating these critical transitions remains challenging in systems with many species because the associated early warning signals can be weakly present or even absent in some species, depending on the system dynamics. Therefore, our limited knowledge of ecological dynamics may suggest that it is hard to identify those species in the system that display early warning signals. Here, we show that, in mutualistic ecological systems, it is possible to identify species that early anticipate critical transitions by knowing only the system structure-that is, the network topology of plant-animal interactions. Specifically, we leverage the mathematical theory of structural observability of dynamical systems to identify a minimum set of "sensor species," whose measurement guarantees that we can infer changes in the abundance of all other species. Importantly, such a minimum set of sensor species can be identified by using the system structure only. We analyzed the performance of such minimum sets of sensor species for detecting early warnings using a large dataset of empirical plant-pollinator and seed-dispersal networks. We found that species that are more likely to be sensors tend to anticipate earlier critical transitions than other species. Our results underscore how knowing the structure of multispecies systems can improve our ability to anticipate critical transitions.

Trophic and spatial complementarity on seed dispersal services by birds, wild mammals, and cattle in a Mediterranean woodland pasture

Most earth surfaces have undergone intensive land-use changes, creating habitat mosaics. Seed dispersal by animals is a crucial process in such mosaics, but community-wide studies comparing the functional complementarity and response to man-imposed habitat heterogeneity are rare. Here, we investigate the trophic and spatial seed dispersal networks underpinning a strong, woody vegetation expansion over a pastureland inside the largest forest remnant in western Sicily, Italy. Over two fruiting seasons, we surveyed transects in three distinct biomes within our study area: forest, pastureland, and unpaved road. In total, we collected 659 feces and tested for differences in defecation patterns and seed rain density of birds, wild mammals, and cattle. We also tested the degree of trophic and spatial specialization and modularity using a network approach. Overall, birds dispersed 1208 seeds/ha of nine plant species, including six exclusive. Mammals dispersed 679 seeds/ha from four wild species, three of which also dispersed by birds, and 38 seeds/ha of three cultivated species. In turn, mammals dispersed exclusively the seeds of wild pear ( Pyrus amygdaliformis ), the most abundant tree in the woodland pasture. Cattle only dispersed wild pear, but accounting for 56% of the dispersed seeds. Seed rain densities were significantly higher in woodland pastures than in forests. However, almost of half the seeds dispersed by cattle and red fox were deposited on unpaved roads. While both trophic and spatial networks were more specialized than expected, we did detect distinct modules. Our study demonstrated the magnitude of the effects of man-made habitat heterogeneity on seed dispersal services, giving baseline information for restoration programs as well as high nature value pastureland management strategies. • Birds and mammals are complementary in their seed dispersal services and key for vegetation dynamics. • Rewilding with cattle can just partially compensate this services, but not replace wild mammals role. • Fruit-rich woodland pasture was more relevant than fruit poor managed forest for seed dispersal networks. • Soft linear developments may act both as seed dispersal corridors or as seed dispersal sinks. • Seed dispersal networks can be good indicators to define high nature value agroforestry systems.

Bottom-up cascading effects of quarry revegetation deplete bird-mediated seed dispersal services

Quarrying activities cause profound modifications on ecosystems, such as removal of vegetation cover, biodiversity loss and depletion of ecosystem services. Ecological restoration stands as a solution to revert such effects. Concomitantly, awareness is currently being given on ecosystem services and ecological processes to evaluate restoration efficiency.The objective of the study was to assess restoration success in a quarry subjected to restoration practices for the last 40 years involving the plantation of native Mediterranean vegetation and the non-native Aleppo pine Pinus halepensis. The study was carried out by assessing the effectiveness of seed dispersal service provided by birds in the restored quarry by comparing this service to neighbouring natural (shrubland) and other semi-natural areas (oak-pine mixed open and Aleppo pine forest) present at the landscape. For this purpose, we explored bird composition structure and seed dispersal networks using point counts and faecal samples of mist-netted birds. We also collected vegetation structure data and explored its effect on bird community composition.Our results showed that bird abundance in the restored quarry was significantly lower, and its bird community was compositionally different than natural shrubland and semi-natural areas. For instance, seed-dispersing birds, woody and shrub/ground foragers and partially migrators were the most affected groups at the restored area. Bird community composition and their traits were likely driven by vegetation characteristics, with higher native vegetation cover and fruit richness promoting higher bird abundance and Aleppo pine cover negatively influencing seed-dispersing birds. Concurrently, seed dispersal network in the restored quarry was less complex than in other areas.Seed dispersal services in the restored quarry were below the reported values for neighbouring natural and semi-natural areas and are likely driven by the low abundance of seed-dispersing birds. We consider that the causes affecting this group's low abundance can be related to revegetation measures favouring Aleppo pine, combined with a shallow soil depth and poor soil quality, which may have constrained native vegetation development.We conclude that seed dispersal services at the quarry are depleted, which may suggest a low restoration success concerning ecosystem functioning. Our results strengthen that quarry revegetation with non-native species must be avoided, since it alters bird community composition, and consequently, affects seed dispersal service provided by birds.

Deforestation Simplifies Understory Bird Seed-Dispersal Networks in Human-Modified Landscapes

Global biodiversity is threatened by land-use changes through human activities. This is mainly due to the conversion of continuous forests into forest fragments surrounded by anthropogenic matrices. In general, sensitive species are lost while species adapted to disturbances succeed in altered environments. However, whether the interactions performed by the persisting species are also modified, and how it scales up to the network level throughout the landscape are virtually unknown in most tropical hotspots of biodiversity. Here we evaluated how landscape predictors (forest cover, total core area, edge density, inter-patch isolation) and local characteristics (fruit availability, vegetation complexity) affected understory birds seed-dispersal networks in 19 forest fragments along the hyperdiverse but highly depauperate northeast distribution of the Brazilian Atlantic Forest. Also, our sampled sites were distributed in two regions with contrasting land cover changes. We used mist nets to obtain samples of understory bird food contents to identify the plant species consumed and dispersed by them. We estimated network complexity on the basis of the number of interactions, links per species, interaction evenness, and modularity. Our findings showed that the number of interactions increased with the amount of forest cover, and it was significantly lower in the more deforested region. None of the other evaluated parameters were affected by any other landscape or local predictors. We also observed a lack of significant network structure compared to null models, which we attribute to a pervasive impoverishment of bird and plant communities in these highly modified landscapes. Our results demonstrate the importance of forest cover not only to maintain species diversity but also their respective mutualistic relationships, which are the bases for ecosystem functionality, forest regeneration and the provision of ecological services.

The evolution of ecological networks

Evolutionary Ecology Plants and the animals that eat their fruits and disperse their seeds form complex networks of mutualistic interactions. The structures of many such networks and the ecological forces that shape them are well known, but their deeper evolutionary history has received little attention. Burin et al. address this knowledge gap in a study of frugivorious bird species in documented seed-dispersal networks around the world (see the Perspective by Bello and Barreto). Species occupying central positions in frugivory networks, which thus interact with many plant species, tend to belong to lineages that are more stable over macroevolutionary time scales. These patterns are more evident in regions with warmer and wetter climates and provide evidence that evolutionary processes can leave a signal on the structure of current ecological networks. Science , this issue p. [733][1] see also p. [682][2] [1]: /lookup/doi/10.1126/science.abf0556 [2]: /lookup/doi/10.1126/science.abi8160

Species functional traits and abundance as drivers of multiplex ecological networks: first empirical quantification of inter-layer edge weights.

Many vertebrate species act as both plant pollinators and seed-dispersers, thus interconnecting these processes, particularly on islands. Ecological multilayer networks are a powerful tool to explore interdependencies between processes; however, quantifying the links between species engaging in different types of interactions (i.e. inter-layer edges) remains a great challenge. Here, we empirically measured inter-layer edge weights by quantifying the role of individually marked birds as both pollinators and seed-dispersers of Galápagos plant species over an entire year. Although most species (80%) engaged in both functions, we show that only a small proportion of individuals actually linked the two processes, highlighting the need to further consider intra-specific variability in individuals' functional roles. Furthermore, we found a high variation among species in linking both processes, i.e. some species contribute more than others to the modular organization of the multilayer network. Small and abundant species are particularly important for the cohesion of pollinator seed-dispersal networks, demonstrating the interplay between species traits and neutral processes structuring natural communities.

Accelerating homogenization of the global plant-frugivore meta-network.

Introductions of species by humans are causing the homogenization of species composition across biogeographic barriers1-3. The ecological and evolutionary consequences of introduced species derive from their effects on networks of species interactions4,5, but we lack a quantitative understanding of the impacts of introduced species on ecological networks and their biogeographic patterns globally. Here we address this data gap by analysing mutualistic seed-dispersal interactions from 410 local networks, encompassing 24,455 unique pairwise interactions between 1,631 animal and 3,208 plant species. We show that species introductions reduce biogeographic compartmentalization of the global meta-network, in which nodes are species and links are interactions observed within any local network. This homogenizing effect extends across spatial scales, decreasing beta diversity among local networks and modularity within networks. The prevalence of introduced interactions is directly related to human environmental modifications and is accelerating, having increased sevenfold over the past 75 years. These dynamics alter the coevolutionary environments that mutualists experience6, and we find that introduced species disproportionately interact with other introduced species. These processes are likely to amplify biotic homogenization in future ecosystems7 and may reduce the resilienceof ecosystems by allowing perturbations to propagate more quickly and exposing disparate ecosystems to similar drivers. Our results highlight the importance of managing the increasing homogenization of ecological complexity.

Drivers of bat roles in Neotropical seed dispersal networks: abundance is more important than functional traits.

While functional traits can facilitate or constrain interactions between pair of species in ecological communities, relative abundances regulate the probabilities of encounter among individuals. However, the relative importance of traits and relative abundances for the role species play in seed dispersion networks remains poorly explored. Here, we analyzed 20 Neotropical seed dispersal networks distributed from Mexico to southeastern Brazil to evaluate how relativeabundance and functional traits influence batspecies' roles in seed dispersal networks. We tested how bat relativeabundance and traits relate to species contribution to between-module (c metric) and within-module connectivity (z metric) and their position and potential to mediate indirect effects between species (betweenness centrality). Our results indicate that relative abundance is the main determinant of the role bats play in the networks, while traits such as aspect ratio show modest yet statistically significant importance in predicting specific roles. Moreover, all seed dispersal networks presented two or three superabundant obligatory frugivore species that interacted with a high number of plants. The modest influence of the functional traits on species' roles is likely related to the low variation of morphological traits related to foraging ecology, which reduces the chances of morphological mismatching between consumers and resources in the system. In this scenario, abundant bats have higher chances of encountering resources and being capable of consuming them which leads such species to play critical roles in the community by acting as module hubs and network connectors.

Similar composition of functional roles in Andean seed-dispersal networks, despite high species and interaction turnover.

The species composition of local communities varies in space, and its similarity generally decreases with increasing geographic distance between communities, a phenomenon known as distance decay of similarity. It is, however, not known how changes in local species composition affect ecological processes, that is, whether they lead to differences in the local composition of species' functional roles. We studied eight seed-dispersal networks along the South American Andes and compared them with regard to their species composition and their composition of functional roles. We tested (1) if changes in bird species composition lead to changes in the composition of bird functional roles, and (2) if the similarity in species composition and functional-role composition decreased with increasing geographic distance between the networks. We also used cluster analysis to (3) identify bird species with similar roles across all networks based on the similarity in the plants they consume, (i) considering only the species identity of the plants and (ii) considering the functional traits of the plants. Despite strong changes in species composition, the networks along the Andes showed similar composition of functional roles. (1) Changes in species composition generally did not lead to changes in the composition of functional roles. (2) Similarity in species composition, but not functional-role composition, decreased with increasing geographic distance between the networks. (3) The cluster analysis considering the functional traits of plants identified bird species with similar functional roles across all networks. The similarity in functional roles despite the high species turnover suggests that the ecological process ofseed dispersalis organized similarly along the Andes, with similar functional roles fulfilled locally by different sets of species. The high species turnover, relative to functional turnover, also indicates that a large number of bird species are needed to maintain the seed-dispersal process along the Andes.

Downsizing of animal communities triggers stronger functional than structural decay in seed-dispersal networks

Downsizing of animal communities due to defaunation is prevalent in many ecosystems. Yet, we know little about its consequences for ecosystem functions such as seed dispersal. Here, we use eight seed-dispersal networks sampled across the Andes and simulate how downsizing of avian frugivores impacts structural network robustness and seed dispersal. We use a trait-based modeling framework to quantify the consequences of downsizing—relative to random extinctions—for the number of interactions and secondary plant extinctions (as measures of structural robustness) and for long-distance seed dispersal (as a measure of ecosystem function). We find that downsizing leads to stronger functional than structural losses. For instance, 10% size-structured loss of bird species results in almost 40% decline of long-distance seed dispersal, but in less than 10% of structural loss. Our simulations reveal that measures of the structural robustness of ecological networks underestimate the consequences of animal extinction and downsizing for ecosystem functioning.

Invasive birds spread native seeds

Ecological Networks When humans introduce exotic species to sensitive ecosystems, invasion and extinction of native species often follow. The resulting ecological communities can develop unusual interactions between the survivors and newcomers. Vizentin-Bugoni et al. analyzed the structure of seed dispersal networks in Hawai'i, where native bird species have been mostly replaced by invaders. They found that the native plants now depend on the invasive birds for seed dispersal. The network of dispersal interactions is complex and stable, which are features of native seed-dispersal networks in other parts of the world. It appears that introduced species may, in some circumstances, become integrated into native ecosystems. Science , this issue p. [78][1] [1]: /lookup/volpage/364/78?iss=6435